Landscape Dynamics Determine the Small-Scale Genetic Structure of An
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Journal of Coastal Research 28 4 780–786 West Palm Beach, Florida July 2012 Landscape Dynamics Determine the Small-Scale Genetic Structure of an Endangered Dune Slack Plant Species Dries Bonte{, Peter Breyne{, Rein Brys{{, Eduardo de la Pen˜a{, Bram D’hondt{, Ce´line Ghyselen{, Martijn L. Vandegehuchte{, and Maurice Hoffmann{{ www.cerf-jcr.org {Ghent University {Research Institute for Nature and Forest Department of Biology Department of Biodiversity and Natural Environment Terrestrial Ecology Unit Kliniekstraat 25 K.L. Ledeganckstraat 35 1070 Brussel, Belgium 9000 Ghent, Belgium [email protected] ABSTRACT Bonte, D.; Breyne, P.; Brys, R.; de la Pen˜ a, E.; D’hondt, B.; Ghyselen, C.; Vandegehuchte, M.L., and Hoffmann, M., 2012. Landscape dynamics determine the small-scale genetic structure of an endangered dune slack plant species. Journal of Coastal Research, 28(4), 780–786. West Palm Beach (Florida), ISSN 0749-0208. Understanding the processes that determine genetic variation within landscapes is a crucial factor for successful management of threatened plant species that are sensitive to both environmental and genetic bottlenecks. While current insights point to the importance of historical landscape processes for the genetic structure of populations at large spatial scales, their relevance at small spatial scales has been largely neglected. In this context, coastal dunes are a typical example of dynamic and geologically young landscapes in which current and historical sand drift may have strong impacts on the spatial dynamics of a large number of plant species. One of these is the endangered plant species Parnassia palustris, typically inhabiting dune slacks formed by recent sand displacements in parabolic dune landscapes. Dune slacks originating from the same sand drift process are located within the same parabola unit. The species is known to suffer from dispersal limitation and from inbreeding when genetic exchange between populations is restricted. By means of amplified fragment length polymorphism, we demonstrate that the species shows a genetic substructuring both at the level of the metapopulation and the local landscape. Populations located within the same parabola unit are much more closely related than expected on the basis of geographic distance. Moreover, population size is related to genetic diversity within populations. The species’ population genetic structure should consequently be regarded as a shifting mosaic of genetic variation, mediated by sand drift driven landscape formation. Therefore, the maintenance of sand dynamics is essential to preserve genetic diversity in dynamic dune landscapes. ADDITIONAL INDEX WORDS: AFLP, metapopulation, Parnassia palustris, population size, sand dynamics. INTRODUCTION biology (Manel et al., 2003). Recent population genetic studies have demonstrated the relationship between population size, Understanding the processes and patterns of gene flow and distance between populations, and genetic differentiation local adaptation requires a detailed knowledge of how among populations, which is strongly affected by the species’ landscape characteristics affect the genetic structure of set of life history traits (see, e.g., Hamrick and Godt, 1996; populations (Holderegger and Wagner, 2008). This is especially Honnay and Jacquemyn 2007; Nybom and Bartish, 2000 for true for plants, in which the process of gene flow is often comprehensive reviews). In contrast, only few studies have strongly influenced by the configuration of the surrounding explicitly tested how landscape genesis (i.e., processes that landscape and prevented by the barriers within it (Sork et al., shape the landscape configuration) may affect spatial patterns 1999). This understanding is crucial, not only to improve in neutral genetic variation, underlying microevolutionary general insights on genetics in conservation biology, but also to processes, and the eventual feedback on life history traits properly manage endangered species in order to maintain and (Balkenhol et al., 2009; Storfer et al., 2007). restore the genetic diversity of their populations. Approaches In general, studies aiming to test the relative importance of from so-called landscape genetics (Holderegger and Wagner historicalvs.currentgeneflowinrelationtolandscapegenesisare 2008) promise to facilitate our understanding of how geograph- constrained by the fact that the configuration of most landscapes ic and environmental features may affect genetic variation at to date is heavily influenced by anthropogenic factors on a very both the population and individual level and may have short timescale relative to most natural processes of landscape important implications for ecology, evolution, and conservation formation. Therefore, the observed genetic variation of these populations often does not confirm general predictions of (meta-) population genetic theory, for instance, the fact that genetic DOI: 10.2112/JCOASTRES-D-10-00128.1 received 24 August 2010; accepted in revision 1 November 2010. distance and geographic distance are not always found to be ’ Coastal Education & Research Foundation 2012 related (Bonnin et al., 2002; Leimu et al., 2006). Sand Dynamics and Plant Genetic Structure 781 Landscape formation may induce spatial genetic variation ulation crosses resulting in a higher reproduction capacity than due to historic gene flow and common founder effects and by within-metapopulation crosses, indicated a larger degree of decreasing local population sizes if habitat formation becomes compatibility between plants originating from different meta- restricted. Two consequences of small population size are populations (Bossuyt 2007). By means of amplified fragment increased genetic drift and inbreeding. Genetic drift and length polymorphism (AFLP) analysis, we tested the hypoth- inbreeding may influence small plant populations by changing esis that landscape dynamics (i.e., parabolic dune genesis) are patterns of genetic diversity. Genetic drift decreases genetic important drivers of genetic differentiation in P. palustris variation within populations, while it generally increases within existing metapopulations relative to among-metapopu- differentiation among populations, an effect that becomes lation differentiation. more pronounced in declining populations (Barrett and Kohn, 1991; Ellstrand and Elam, 1993; Young, Boyle, and Brown, MATERIAL AND METHODS 1996). Inbreeding increases homozygosity within populations, whereas smaller populations lose genetic variation faster than Study Species larger populations (Ellstrand and Elam, 1993). The expected Parnassia palustris (Saxifragaceae) is a perennial herb with relationship between population size and genetic diversity is, a circumboreal distribution (Bonnin et al., 2002; Borgen and however, often missing (Bonnin et al., 2002; Leimu et al., 2006) Hultga˚rd, 2003). Each plant has basal leaves and 1–30 because populations occur in human managed habitats that flowering stems, each with one terminal flower. The species could have experienced dramatic short-term changes. As is hermaphroditic and protandrous. The five stamens sequen- Bonnin et al. (2002) suggest, these changes may include tially discharge their pollen before the stigma becomes bottlenecks and a changing degree of connection to other receptive. It is usually cross-pollinated and rarely autoga- populations (Holderegger and Wagner, 2008). mously pollinated (Martens, 1936). The species is mainly In dynamic landscapes, landscape genesis is by definition a outcrossing and strongly depends on pollinators for optimal geologically young process that can often be disentangled from pollination and seed set (Sandvik and Totland, 2003). Parnas- human interference on habitat configuration. Coastal dunes sia palustris is insect pollinated, mainly by Diptera, particu- along the North Sea comprise such a system. Owing to sand larly hoverflies (Syrphidae), but other insects contribute to drift dynamics, dry parabolic dune ridges are continuously pollen transfer (Sandvik and Totland, 2003). It flowers from shifting in a northeasterly direction, leaving behind young August through September, and fruits, containing several ephemeral dune slacks (Provoost, Jones, and Edmondson, hundreds of seeds, ripen from September through October. The 2009), whose ecological characteristics are often determined by small, light seeds are dispersed by water and wind. Parnassia the groundwater level and the carbonate content at the palustris is considered endangered in northern France, moment of development. Here, several plant species find their Luxembourg, Belgium, and the Netherlands (Bonnin et al., optimal, though temporary, growing conditions; they are often 2002), where it is a rare plant in lime-rich dune slacks along the restricted to specific environmental conditions in space and coast and inland lime-rich marshes. time. Their populations are subsequently expected to be predominantly linked to the historical dynamics of these Study Area landscapes, in which gene flow patterns are strongly deter- mined by the occurrence of dry parabolic dune ridges that may The study was conducted in a sandy dune area along the function as effective dispersal barriers. On the other hand, the western Belgian and northeastern French coast. This area has fragmentation of larger dune entities due to the steady increase been extensively fragmented by human activities since the of urbanized areas is another factor that may induce genetic beginning of the 20th century. The remaining dune